Task-Demand-Dependent Neural Representation of Odor Information in the Olfactory Bulb and Posterior Piriform Cortex

Abstract

In awake rodents, the neural representation of olfactory information in the olfactory bulb is largely dependent on brain state and behavioral context. Learning-modified neural plasticity has been observed in mitral/tufted cells, the main output neurons of the olfactory bulb. Here, we propose that the odor information encoded by mitral/tufted cell responses in awake mice is highly dependent on the behavioral task demands. We used fiber photometry to record calcium signals from the mitral/tufted cell population in awake, head-fixed male mice under different task demands. We found that the mitral/tufted cell population showed similar responses to two distinct odors when the odors were presented in the context of a go/go task, in which the mice received a water reward regardless of the identity of the odor presented. However, when the same odors were presented in a go/no-go task, in which one odor was rewarded and the other was not, then the mitral cell population responded very differently to the two odors, characterized by a robust reduction in the response to the nonrewarded odor. Thus, the representation of odors in the mitral/tufted cell population depends on whether the task requires discrimination of the odors. Strikingly, downstream of the olfactory bulb, pyramidal neurons in the posterior piriform cortex also displayed a task-demand-dependent neural representation of odors, but the anterior piriform cortex did not, indicating that these two important higher olfactory centers use different strategies for neural representation.

SIGNIFICANCE STATEMENT The most important task of the olfactory system is to generate a precise representation of odor information under different brain states. Whether the representation of odors by neurons in olfactory centers such as the olfactory bulb and the piriform cortex depends on task demands remains elusive. We find that odor representation in the mitral/tufted cells of the olfactory bulb depends on whether the task requires odor discrimination. A similar neural representation is found in the posterior piriform cortex but not the anterior piriform cortex, indicating that these higher olfactory centers use different representational strategies. The task-demand-dependent representational strategy is likely important for facilitating information processing in higher brain centers responsible for decision making and encoding of salience.